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PMID: 16421253 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Rab1 defines a novel pathway connecting the pre-Golgi intermediate compartment with the cell periphery.

Molecular biology of the cell ·Vol. 17 ·No. 4 ·2006-04-00 ·Pages 1514-26

Sannerud R, Marie M, Nizak C, Dale HA, Pernet-Gallay K, Perez F, Goud B, Saraste J

Abstract

The function of the pre-Golgi intermediate compartment (IC) and its relationship with the endoplasmic reticulum (ER) and Golgi remain only partially understood. Here, we report striking segregation of IC domains in polarized PC12 cells that develop neurite-like processes. Differentiation involves expansion of the IC and movement of Rab1-containing tubules to the growth cones of the neurites, whereas p58- and COPI-positive IC elements, like rough ER and Golgi, remain in the cell body. Exclusion of Rab1 effectors p115 and GM130 from the neurites further indicated that the centrifugal, Rab1-mediated pathway has functions that are not directly related to ER-to-Golgi trafficking. Disassembly of COPI coats did not affect this pathway but resulted in missorting of p58 to the neurites. Live cell imaging showed that green fluorescent protein (GFP)-Rab1A-containing IC elements move bidirectionally both within the neurites and cell bodies, interconnecting different ER exit sites and the cis-Golgi region. Moreover, in nonpolarized cells GFP-Rab1A-positive tubules moved centrifugally towards the cell cortex. Hydroxymethylglutaryl-CoA reductase, the key enzyme of cholesterol biosynthesis, colocalized with slowly sedimenting, Rab1-enriched membranes when the IC subdomains were separated by velocity sedimentation. These results reveal a novel pathway directly connecting the IC with the cell periphery and suggest that this Rab1-mediated pathway is linked to the dynamics of smooth ER.

MeSH Terms
Animals Cell Compartmentation Cell Polarity Dogs Endoplasmic Reticulum/metabolism Endoplasmic Reticulum Chaperone BiP Golgi Apparatus/metabolism Heat-Shock Proteins/analysis,metabolism Humans Mannose-Binding Lectins/analysis,metabolism Membrane Proteins/analysis,metabolism Molecular Chaperones/analysis,metabolism Nerve Growth Factor/pharmacology Neurites/chemistry,metabolism,physiology Neurons/chemistry,cytology,drug effects PC12 Cells Phosphoprotein Phosphatases/analysis,metabolism Protein Transport Rats Transfection rab1 GTP-Binding Proteins/analysis,metabolism
Chemicals
Endoplasmic Reticulum Chaperone BiP Heat-Shock Proteins Lman1 protein, rat Mannose-Binding Lectins Membrane Proteins Molecular Chaperones Nerve Growth Factor HMG-CoA reductase phosphatase Phosphoprotein Phosphatases rab1 GTP-Binding Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Sannerud Ragna
Section of Anatomy and Cell Biology, Department of Biomedicine, University of Bergen, N-5009 Bergen, Norway.
Marie Michaël
Nizak Clément
Dale Hege Avsnes
Pernet-Gallay Karin
Perez Franck
Goud Bruno
Saraste Jaakko
References (79)
79 references, click to expand
  1. Retrograde traffic in the biosynthetic-secretory route: pathways and machinery.
    Curr Opin Cell Biol. 2003 Aug;15(4):438-45 PMID: 12892784
  2. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains.
    Dev Cell. 2003 Oct;5(4):583-94 PMID: 14536060
  3. Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons.
    J Cell Sci. 2004 Jan 15;117(Pt 2):163-75 PMID: 14676272
  4. Endoplasmic reticulum export site formation and function in dendrites.
    J Neurosci. 2004 Apr 14;24(15):3770-6 PMID: 15084657
  5. Misfolded proinsulin accumulates in expanded pre-Golgi intermediates and endoplasmic reticulum subdomains in pancreatic beta cells of Akita mice.
    FASEB J. 2004 May;18(7):917-9 PMID: 15033933
  6. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.
    Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424-8 PMID: 1065897
  7. Fine structure of initial outgrowth of processes induced in a pheochromocytoma cell line (PC12) by nerve growth factor.
    J Neurocytol. 1979 Aug;8(4):493-511 PMID: 490193
  8. Ultrastructural analysis of crystalloid endoplasmic reticulum in UT-1 cells and its disappearance in response to cholesterol.
    J Cell Sci. 1983 Sep;63:1-20 PMID: 6685129
  9. Nerve growth factor induced changes in the Golgi apparatus of PC-12 rat pheochromocytoma cells as studied by ligand endocytosis, cytochemical and morphometric methods.
    J Neurocytol. 1983 Oct;12(5):751-66 PMID: 6139421
  10. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface.
    Cell. 1984 Sep;38(2):535-49 PMID: 6432345
  11. The neuronal endomembrane system. III. The origins of the axoplasmic reticulum and discrete axonal cisternae at the axon hillock.
    J Neurosci. 1985 Dec;5(12):3135-44 PMID: 3878394
  12. Lovastatin, an inhibitor of cholesterol synthesis, induces hydroxymethylglutaryl-coenzyme A reductase directly on membranes of expanded smooth endoplasmic reticulum in rat hepatocytes.
    Proc Natl Acad Sci U S A. 1988 Jul;85(14):5264-8 PMID: 3293052
  13. Morphological and biochemical evidence showing neuronal properties in AtT-20 cells and their growth cones.
    Eur J Cell Biol. 1989 Aug;49(2):259-73 PMID: 2506049
  14. Low temperature-induced transport blocks as tools to manipulate membrane traffic.
    Methods Cell Biol. 1989;32:257-74 PMID: 2691852
  15. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane.
    J Biol Chem. 1990 Feb 5;265(4):1919-23 PMID: 2153669
  16. Isolation of functional Golgi-derived vesicles with a possible role in retrograde transport.
    J Cell Biol. 1998 Feb 9;140(3):541-51 PMID: 9456315
  17. Neuronal calcium signaling.
    Neuron. 1998 Jul;21(1):13-26 PMID: 9697848
  18. Retrograde transport from the pre-Golgi intermediate compartment and the Golgi complex is affected by the vacuolar H+-ATPase inhibitor bafilomycin A1.
    Mol Biol Cell. 1998 Dec;9(12):3561-78 PMID: 9843588
  19. Molecular mechanisms of neurite extension.
    Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):387-94 PMID: 10212488
  20. Intracellular cholesterol transport.
    Biochim Biophys Acta. 1999 Apr 19;1438(1):19-37 PMID: 10216277
  21. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles.
    Cell. 1999 Jul 9;98(1):81-90 PMID: 10412983
  22. Segregation of COPI-rich and anterograde-cargo-rich domains in endoplasmic-reticulum-to-Golgi transport complexes.
    Curr Biol. 1999 Jul 29-Aug 12;9(15):821-4 PMID: 10469566
  23. Neurite extension occurs in the absence of regulated exocytosis in PC12 subclones.
    Mol Biol Cell. 1999 Sep;10(9):2919-31 PMID: 10473636
  24. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments.
    Nat Cell Biol. 2004 Nov;6(11):1071-81 PMID: 15502824
  25. Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment.
    J Cell Biol. 1995 Dec;131(6 Pt 1):1403-19 PMID: 8522600
  26. Coupling of ER exit to microtubules through direct interaction of COPII with dynactin.
    Nat Cell Biol. 2005 Jan;7(1):48-55 PMID: 15580264
  27. Live imaging of bidirectional traffic from the ERGIC.
    J Cell Sci. 2005 Jan 15;118(Pt 2):357-67 PMID: 15632110
  28. The MICAL proteins and rab1: a possible link to the cytoskeleton?
    Biochem Biophys Res Commun. 2005 Mar 11;328(2):415-23 PMID: 15694364
  29. Ribophorin I associates with a subset of membrane proteins after their integration at the sec61 translocon.
    J Biol Chem. 2005 Feb 11;280(6):4195-206 PMID: 15556939
  30. Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration.
    Biochemistry. 2005 Apr 19;44(15):5816-26 PMID: 15823040
  31. Heme deficiency interferes with the Ras-mitogen-activated protein kinase signaling pathway and expression of a subset of neuronal genes.
    Cell Growth Differ. 2002 Sep;13(9):431-9 PMID: 12354752
  32. Ultrastructural characterization of endoplasmic reticulum--Golgi transport containers (EGTC).
    J Cell Sci. 2002 Nov 15;115(Pt 22):4263-73 PMID: 12376558
  33. Colocalization of Ca2+-ATPase and GRP94 with p58 and the effects of thapsigargin on protein recycling suggest the participation of the pre-Golgi intermediate compartment in intracellular Ca2+ storage.
    Eur J Cell Biol. 2002 Sep;81(9):469-83 PMID: 12416724
  34. ER to Golgi transport: Requirement for p115 at a pre-Golgi VTC stage.
    J Cell Biol. 1999 Dec 13;147(6):1205-22 PMID: 10601335
  35. ERGIC-53 and traffic in the secretory pathway.
    J Cell Sci. 2000 Feb;113 ( Pt 4):587-96 PMID: 10652252
  36. Mammalian homologues of yeast sec31p. An ubiquitously expressed form is localized to endoplasmic reticulum (ER) exit sites and is essential for ER-Golgi transport.
    J Biol Chem. 2000 May 5;275(18):13597-604 PMID: 10788476
  37. COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites.
    J Cell Sci. 2000 Jun;113 ( Pt 12):2177-85 PMID: 10825291
  38. Transport between ER and Golgi.
    Curr Opin Cell Biol. 2000 Aug;12(4):445-9 PMID: 10873822
  39. Dissecting the role of the golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8375-80 PMID: 10890900
  40. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion.
    Science. 2000 Jul 21;289(5478):444-8 PMID: 10903204
  41. Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes.
    Cell. 2000 Aug 4;102(3):315-23 PMID: 10975522
  42. Dynamics of transitional endoplasmic reticulum sites in vertebrate cells.
    Mol Biol Cell. 2000 Sep;11(9):3013-30 PMID: 10982397
  43. The p58-positive pre-golgi intermediates consist of distinct subpopulations of particles that show differential binding of COPI and COPII coats and contain vacuolar H(+)-ATPase.
    J Cell Sci. 2000 Oct;113 ( Pt 20):3623-38 PMID: 11017878
  44. Secretory protein trafficking and organelle dynamics in living cells.
    Annu Rev Cell Dev Biol. 2000;16:557-89 PMID: 11031247
  45. Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis--Golgi tethering.
    Traffic. 2001 Apr;2(4):268-76 PMID: 11285137
  46. The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b.
    EMBO Rep. 2001 Apr;2(4):336-41 PMID: 11306556
  47. Endoplasmic reticulum of animal cells and its organization into structural and functional domains.
    Int Rev Cytol. 2001;205:149-214 PMID: 11336391
  48. ER export: public transportation by the COPII coach.
    Curr Opin Cell Biol. 2001 Aug;13(4):438-43 PMID: 11454450
  49. Immunolocalization of UDP-glucose:glycoprotein glucosyltransferase indicates involvement of pre-Golgi intermediates in protein quality control.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10710-5 PMID: 11535823
  50. Structural complexity and functional diversity of endoplasmic reticulum Ca(2+) stores.
    Trends Neurosci. 2001 Oct;24(10):602-8 PMID: 11576675
  51. The GM130 and GRASP65 Golgi proteins cycle through and define a subdomain of the intermediate compartment.
    Nat Cell Biol. 2001 Dec;3(12):1101-13 PMID: 11781572
  52. Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion.
    Immunity. 2003 Feb;18(2):243-53 PMID: 12594951
  53. Membrane domains in the secretory and endocytic pathways.
    Cell. 2003 Feb 21;112(4):507-17 PMID: 12600314
  54. COPI recruitment is modulated by a Rab1b-dependent mechanism.
    Mol Biol Cell. 2003 May;14(5):2116-27 PMID: 12802079
  55. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging.
    J Neurosci. 2003 Jul 16;23(15):6188-99 PMID: 12867502
  56. Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately.
    J Cell Biol. 1990 May;110(5):1501-11 PMID: 2335560
  57. Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments.
    J Cell Biol. 1991 Oct;115(1):31-43 PMID: 1918138
  58. Distribution of the intermediate elements operating in ER to Golgi transport.
    J Cell Sci. 1991 Nov;100 ( Pt 3):415-30 PMID: 1808196
  59. GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex.
    J Cell Biol. 1992 Nov;119(4):749-61 PMID: 1429835
  60. Subcompartments of the endoplasmic reticulum.
    Semin Cell Biol. 1992 Oct;3(5):325-41 PMID: 1457776
  61. Pathways of protein sorting and membrane traffic between the rough endoplasmic reticulum and the Golgi complex.
    Semin Cell Biol. 1992 Oct;3(5):343-55 PMID: 1457777
  62. Characterization of a 58 kDa cis-Golgi protein in pancreatic exocrine cells.
    J Cell Sci. 1992 Oct;103 ( Pt 2):321-33 PMID: 1478936
  63. Protein targeting in the neuron.
    Annu Rev Neurosci. 1993;16:95-127 PMID: 8460907
  64. A three-dimensional reconstruction study of the rough ER-Golgi interface in serial thin sections of the pancreatic acinar cell of the rat.
    J Cell Sci. 1994 Mar;107 ( Pt 3):517-28 PMID: 8006070
  65. Continuous network of endoplasmic reticulum in cerebellar Purkinje neurons.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7510-4 PMID: 7519781
  66. A possible role for stable microtubules in intracellular transport from the endoplasmic reticulum to the Golgi apparatus.
    J Cell Sci. 1994 May;107 ( Pt 5):1321-31 PMID: 7929638
  67. Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1557-74 PMID: 7798312
  68. Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1541-52 PMID: 7615674
  69. The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons.
    Mol Biol Cell. 1995 Oct;6(10):1315-32 PMID: 8573789
  70. Regulation of organelle biogenesis.
    Cell. 1996 Feb 9;84(3):389-94 PMID: 8608592
  71. Organelle inheritance.
    Cell. 1996 Feb 9;84(3):395-400 PMID: 8608593
  72. Molecular cloning and expression of a 58-kDa cis-Golgi and intermediate compartment protein.
    J Biol Chem. 1996 Feb 23;271(8):4031-7 PMID: 8626736
  73. Transport of an external Lys-Asp-Glu-Leu (KDEL) protein from the plasma membrane to the endoplasmic reticulum: studies with cholera toxin in Vero cells.
    J Cell Biol. 1996 May;133(4):777-89 PMID: 8666663
  74. Segregation of ERGIC53 and the mammalian KDEL receptor upon exit from the 15 degrees C compartment.
    Eur J Cell Biol. 1995 Dec;68(4):398-410 PMID: 8690019
  75. The economics of neurite outgrowth--the addition of new membrane to growing axons.
    Trends Neurosci. 1996 Apr;19(4):144-9 PMID: 8658598
  76. ER-to-Golgi transport visualized in living cells.
    Nature. 1997 Sep 4;389(6646):81-5 PMID: 9288971
  77. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane.
    Mol Biol Cell. 1997 Sep;8(9):1805-14 PMID: 9307975
  78. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI.
    Cell. 1997 Sep 19;90(6):1137-48 PMID: 9323141
  79. Golgins in the structure and dynamics of the Golgi apparatus.
    Curr Opin Cell Biol. 2003 Aug;15(4):405-13 PMID: 12892780
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.e05-08-0792
Published
2006-04-00
Epub
2006-00-18
Pages
1514-26
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1415313
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.e05-08-0792 PMC Full Text View journal details
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